Evidence for progenitorderivative speciation in sexually deceptive orchids

Annals of Botany

Volumn 108, Issue 5, 2011, Pages 895-906

  Schlter, Philipp M ^a,b   Ruas, Paulo M ^a,c   Kohl, Gudrun ^a   Ruas, Claudete F ^a,c   Stuessy, Tod F ^a   Paulus, Hannes F ^a  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c STATE UNIVERSITY OF LONDRINA   (Brazil)

Author keywords

AFLP; genetic diversity; genetic structure; low copy nuclear genes; Ophrys; pollination; progenitorderivative speciation; sexually deceptive orchids

Indexed keywords

DNA FINGERPRINTING; GENETIC STRUCTURE; GENETIC VARIATION; GENOME; GEOGRAPHICAL VARIATION; MIMICRY; MONOCOTYLEDON; POLLINATOR; POLYMORPHISM; SPECIATION (BIOLOGY);

OPHRYS; OPHRYS FUSCA; ORCHIDACEAE;

PLANT DNA;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; ARTICLE; CLASSIFICATION; DNA FINGERPRINTING; GENETIC VARIABILITY; GENETICS; GEOGRAPHY; GREECE; GROWTH, DEVELOPMENT AND AGING; HYBRIDIZATION; NUCLEOTIDE SEQUENCE; ORCHIDACEAE; PLANT GENE; POLLINATION; SOUTHERN EUROPE; SPECIES DIFFERENCE; SPECIES DIFFERENTIATION;

AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; BASE SEQUENCE; DNA FINGERPRINTING; DNA, PLANT; GENES, PLANT; GENETIC SPECIATION; GENETIC VARIATION; GEOGRAPHY; GREECE; HYBRIDIZATION, GENETIC; MEDITERRANEAN REGION; ORCHIDACEAE; POLLINATION; SPECIES SPECIFICITY;

EID: 80053251284     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr239     Document Type: Article

References (81)

1. Agren L, Kullenberg B, Sensenbaugh T. 1984. Congruences in pilosity between three species of Ophrys (Orchidaceae) and their hymenopteran pollinators. Nova Acta Regiae Societatis Scientiarum Upsaliensis Ser. V, C, 3: 15-25.
2. Ayasse M, Paxton RJ, TengoJ. 2001. Mating behavior and chemical communication in the order Hymenoptera. Annual Review of Entomology 46: 31-78. (Pubitemid 32304983)
3. Ayasse M, Stokl J, Francke W. 2011. Chemical ecology and pollinatordriven speciation in sexually deceptive orchids. Phytochemistry 72: 1667-1677.
4. Bateman RM, Hollingsworth PM, Preston J, Yi-Bo L, Pridgeon AM, Chase MW. 2003. Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society 142: 1-40. (Pubitemid 36608173)
5. Benham JJ, Jeung J-U, Jasieniuk MA, Kanazin V, Blake TK. 1999. Genographer: a graphical tool for automated fluorescent AFLP and microsatellite analysis. Journal of Agricultural Genomics 4: paper 399.
6. Bernardos S, Cresp A, del Rey F, Amich F. 2005. The section Pseudophrys (Ophrys, Orchidaceae) in the Iberian Peninsula: a morphometric and molecular analysis. Botanical Journal of the Linnean Society 148: 359-375. (Pubitemid 40962697)
7. Bonin A, Bellemain E, Bronken Eidesen P, Pompanon F, Brochmann C, Taberlet P. 2004. How to track and assess genotyping errors in population genetic studies. Molecular Ecology 13: 3261-3273. (Pubitemid 39415663)
8. Bower CC, Brown GR. 2009. Pollinator specificity, cryptic species and geographical patterns in pollinator responses to sexually deceptive orchids in the genus Chiloglottis: the Chiloglottis gunnii complex. Australian Journal of Botany 57: 37-55.
9. Caporali E, Grunanger P, Marziani G, Servettaz O, Spada A. 2001. Molecular (RAPD) analysis of some taxa of the Ophrys bertolonii aggregate (Orchidaceae). Israel Journal of Plant Sciences 49: 85-89. (Pubitemid 32824489)
10. Cavalli-Sforza LL, Edwards AWF. 1967. Phylogenetic analysis: models and estimation procedures. Evolution: International Journal of Organic Evolution 21: 550-570.
11. Corander J, Waldmann P, SillanpaaMJ. 2003. Bayesian analysis of genetic differentiation between populations. Genetics 163: 367-374. (Pubitemid 36222679)
12. Cozzolino S, DEmerico S, Widmer A. 2004. Evidence for reproductive isolate selection in Mediterranean orchids: karyotype differences compensate for the lack of pollinator specificity. Proceedings of the Royal Society of London B: Biological Sciences 271: S259-S262. (Pubitemid 38998719)
13. Crawford DJ. 2010. Progenitor-derivative species pairs and plant speciation. Taxon 59: 1413-1423.
14. Delforge P. 2006. Orchids of Europe, North Africa, and the Middle East, 3rd edn. London: A&C Black.
15. Devey DS, Bateman RM, Fay MF, Hawkins JA. 2008. Friends or relatives? Phylogenetics and species delimitation in the controversial European orchid genus Ophrys. Annals of Botany 101: 385-402. (Pubitemid 351197778)
16. Duchesne P, Bernatchez L. 2002. AFLPOP: a computer program for simulated and real population allocation, based on AFLP data. Molecular Ecology Notes 2: 380-383.
17. Ehrendorfer F. 1980. Hybridisierung, Polyploidie und Evolution bei europa isch-mediterranen Orchideen. Die Orchidee Sonderheft: 15-34.
18. Evanno G, Regnout S, Goudet J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14: 2611-2620. (Pubitemid 40886055)
19. Excoffier L, Laval G, Schneider S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1: 47-50.
20. Falush D, Stephens M, Pritchard JR. 2007. Inference of population structure using multilocus genotype data: dominant markers and null alleles. Molecular Ecology Notes 7: 574-578. (Pubitemid 47035522)
21. Gaskett AC. 2011. Orchid pollination by sexual deception: pollinator perspectives. Biological Reviews of the Cambridge Philosophical Society 86: 33-75.
22. Gitzendanner MA, Soltis PS. 2000. Patterns of genetic variation in rare and widespread plant congeners. American Journal of Botany 87: 783-792. (Pubitemid 30411115)
23. Gogler J, Stokl J, Sramkova A, et al. 2009. Menage atrois - two endemic species of deceptive orchids and one pollinator species. Evolution: International Journal of Organic Evolution 63: 2222-2234.
24. Gottlieb LD. 2003. Rethinking classic examples of recent speciation in plants. New Phytologist 161: 71-82. (Pubitemid 38047047)
25. Grunanger P, Caporali E, Marziani G, Menguzzato E, Servettaz O. 1998. Molecular (RAPD) analysis on Italian taxa of the Ophrys bertolonii aggregate (Orchidaceae). Plant Systematics and Evolution 212: 177-184. (Pubitemid 28562768)
26. Gusenleitner F, Schwarz M. 2002. Weltweite Checkliste der Bienengattung Andrena mit Bemerkungen und Erganzungen zu palaarktischen Arten (Hymenoptera, Apidae, Andreninae, Andrena). Entomofauna Supplement 12: 1-1280.
27. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
28. Harrison RG. 1991. Molecular changes at speciation. Annual Review of Ecology and Systematics 22: 281-308. (Pubitemid 21903657)
29. Hutcheson K. 1970. A test for comparing diversities based on the Shannon formula. Journal of Theoretical Biology 29: 151-154.
30. Kretzschmar H, Kretzschmar G, Eccarius W. 2001. Orchideen auf Rhodos. Ein Feldfuhrer durch die Orchideenflora der Insel des Lichts. Bad Hersfeld, Germany: Selbstverlag H. Kretzschmar.
31. Kreutz CAJ. 2003. Feldfuhrer der turkischen Orchideen. Landgraaf, Germany: C. A. J. Kreutz, Selbstverlag.
32. Kullenberg B. 1961. Studies in Ophrys pollination. Zoologiska Bidrag fran Uppsala 34: 1-340.
33. Levin DA. 1993. Local speciation in plants: the rule not the exception. Systematic Botany 18: 197-208.
34. Levin DA. 2004. The ecological transition in speciation. New Phytologist 161: 91-96. (Pubitemid 38047049)
35. Macnair MR, Gardner M. 1998. The evolution of edaphic endemics. In: Howard DJ, Berlocher SH eds. Endless forms: species and speciation. New York: Oxford University Press, 157-171.
36. Magurran AE. 1988. Ecological diversity and its measurement. London: Croom Helm.
37. Mant J, Bower CC, Weston PH, Peakall R. 2005a. Phylogeography of pollinator-specific sexually deceptive Chiloglottis taxa (Orchidaceae): evidence for sympatric divergence? Molecular Ecology 14: 3067-3076.
38. Mant J, Peakall R, Schiestl FP. 2005b. Does selection on floral odor promote differentiation among populations and species of the sexually orchid genus Ophrys? Evolution: International Journal of Organic Evolution 59: 1449-1463. (Pubitemid 41098437)
39. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P. 2010. RDP3: a flexible and fast computer program for analysing recombination. Bioinformatics 26: 2462-2463.
40. Montieri S, Gaudio L, Aceto S. 2004. Isolation of the LFY/FLO homologue in Orchis italica and evolutionary analysis in some European orchids. Gene 333: 101-109. (Pubitemid 38737356)
41. Paulus HF. 2001a. Daten zur Bestaubungsbiologie und Systematik der Gattung Ophrys in Rhodos (Griechenland) mit Beschreibung von Ophrys parvula, Ophrys persephonae, Ophrys lindia, Ophrys eptapigiensis spp. nov. aus der Ophrys fusca s.str. Gruppe und Ophrys cornutula spec. nov. aus der Ophrys oestrifera-Gruppe (Orchidaceae und Insecta, Apoidea). Berichte aus den Arbeitskreisen Heimische Orchideen 18: 38-86.
42. Paulus HF. 2001b. Material zu einer Revision des Ophrys fusca s.str.
43. Artenkreises I. Ophrys nigroaenea-fusca, O. colletes-fusca, O. flavipes-fusca, O. funerea, O. forestieri oder was ist die typische Ophrys fusca Link 1799 (Orchidaceae)? Journal Europaischer Orchideen 33: 121-177.
44. Paulus HF. 2006. Deceived males - pollination biology of the Mediterranean orchid genus Ophrys (Orchidaceae). Journal Europaischer Orchideen 38: 303-353.
45. Paulus HF, Gack C. 1990. Pollinators as prepollinating isolation factors: evolution and speciation in Ophrys (Orchidaceae). Israel Journal of Botany 39: 43-79.
46. Paulus HF, Salkowski H-E. 2007. Bestaubungsbiologische Untersuchungen an Winterorchideen auf der Agais-Insel Kos (Orchidaceae und Insecta, Hymenoptera, Apoidea). Berichte aus den Arbeitskreisen Heimische Orchideen 24: 4-30.
47. Paulus HF, Schluter PM. 2007. Neues aus Kreta und Rhodos: Bestaubungsbiologie und molekular-genetische Trennung in der Ophrys fusca - Gruppe, mit Neubeschreibungen von Ophrys phaidra Paulus nov.sp., O. pallidula Paulus nov.sp. und O. kedra Paulus nov.sp. aus Kreta (Orchidaceae und Insecta, Apoidea). Jahresberichte des Naturwissenschaftlichen Vereins in Wuppertal 60: 101-151.
48. Peakall R, Ebert D, Poldy J, et al. 2010. Pollinator specificity, floral odour chemistry and the phylogeny of Australian sexually deceptive Chiloglottis orchids: implications for pollinator-driven speciation. New Phytologist 188: 437-450.
49. Pedersen H, Faurholdt N. 2007. Ophrys: the bee orchids of Europe. Kew, UK: Kew Publishing.
50. Perron M, Perry DJ, Andalo C, Bousquet J. 2000. Evidence from sequence-tagged-site markers of a recent progenitor-derivative species pair in conifers. Proceedings of the National Academy of Sciences, USA 97: 11331-11336.
51. Pirstinger PM. 1996. Untersuchung der Lippenbehaarung der Gattung Ophrys (Orchidaceae) und ihrer Bestauberweibchen (Apoidea). Mag. rer. nat. thesis, University of Vienna, Vienna, Austria.
52. Pirstinger PM, Paulus HF. 1996. Congruences in pilosity between species of Ophrys (Orchidaceae) and the females of their hymenopteran pollinators (Apoidea). Proceedings of the XX International Congress of Entomology. Firenze, Italy.
53. Ranker TA, Schnabel AF. 1986. Allozymic and morphological evidence for a progenitor-derivative species pair in Camassia (Liliaceae). Systematic Botany 11: 433-445.
54. R Development Core Team. 2010. R: a language and environment for statistical computing. 2.11.0 ed. Vienna, Austria: R Foundation for Statistical Computing. http://www.r-project.org/
55. Rieseberg LH, Brouillet L. 1994. Are many plant species paraphyletic? Taxon 43: 21-32. (Pubitemid 2043202)
56. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
57. Schiestl FP, Ayasse M. 2002. Do changes in floral odor cause speciation in sexually deceptive orchids? Plant Systematics and Evolution 234: 111-119. (Pubitemid 35436637)
58. Schiestl FP, Schluter PM. 2009. Floral isolation, specialized pollination, and pollinator behavior in orchids. Annual Review of Entomology 54: 425-446.
59. Schiestl FP, Ayasse M, Paulus HF, et al. 1999. Orchid pollination by sexual swindle. Nature 399: 421-422.
60. Schiestl FP, Ayasse M, Paulus HF, et al. 2000. Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): patterns of hydrocarbons as the key mechanism for pollination by sexual deception. Journal of Comparative Physiology A 186: 567-574. (Pubitemid 30597115)
61. Schluter D, Conte GL. 2009. Genetics and ecological speciation. Proceedings of the National Academy of Sciences, USA 106: 9955-9962.
62. Schluter PM, Harris SA. 2006. Analysis of multilocus fingerprinting data sets containing missing data. Molecular Ecology Notes 6: 569-572. (Pubitemid 43780795)
63. Schluter PM, Schiestl FP. 2008. Molecular mechanisms of floral mimicry in orchids. Trends in Plant Science 13: 228-235.
64. Schluter PM, Kohl G, Stuessy TF, Paulus HF. 2007a. A screen of low-copy nuclear genes reveals the LFY gene as phylogenetically informative in closely related species of orchids (Ophrys). Taxon 56: 493-504. (Pubitemid 47025842)
65. Schluter PM, Ruas PM, Kohl G, Ruas CF, Stuessy TF, Paulus HF. 2007b. Reproductive isolation in the Aegean Ophrys omegaifera complex (Orchidaceae). Plant Systematics and Evolution 267: 105-119. (Pubitemid 47402426)
66. Schluter PM, Ruas PM, Kohl G, Ruas CF, Stuessy TF, Paulus HF. 2009. Genetic patterns and pollination in Ophrys iricolor and O. mesaritica (Orchidaceae): sympatric evolution by pollinator shift. Botanical Journal of the Linnean Society 159: 583-598.
67. Schluter PM, Xu S, Gagliardini V, et al. 2011. Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids. Proceedings of the National Academy of Sciences, USA 108: 5696-5701.
68. Scopece G, Musacchio A, Widmer A, Cozzolino S. 2007. Patterns of reproductive isolation in Mediterranean orchids. Evolution: International Journal of Organic Evolution 61: 2623-2624.
69. Sinnott RW. 1984. Virtues of the haversine. Sky and Telescope 68: 159.
70. Soliva M, Widmer A. 2003. Gene flow across species boundaries in sympatric, sexually deceptive Ophrys (Orchidaceae) species. Evolution: International Journal of Organic Evolution 57: 2252-2261. (Pubitemid 37388017)
71. Soliva M, Kocyan A, Widmer A. 2001. Molecular phylogenetics of the sexually deceptive orchid genus Ophrys (Orchidaceae) based on nuclear and chloroplast DNA sequences. Molecular Phylogenetics and Evolution 20: 78-88. (Pubitemid 32656903)
72. Stokl J, Schluter PM, Stuessy TF, et al. 2009. Speciation in sexually deceptive orchids: pollinator-driven selection maintains discrete odour phenotypes in hybridizing species. Biological Journal of the Linnean Society 98: 439-451.
73. Takezaki N, Nei M. 1996. Genetic distances and reconstruction of phylogenetic trees from microsatellite DNA. Genetics 144: 389-399. (Pubitemid 26291946)
74. Tremblay RL, Ackerman JD, Zimmerman JK, Calvo RN. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society 84: 1-54. (Pubitemid 40181156)
75. Vereecken NJ. 2009. Deceptive behavior in plants. I. Pollination by sexual deception in orchids: a host-parasite perspective. In: Baluska F, ed. Plant-environment interactions. Heidelberg: Springer Verlag, 203-222.
76. Vos P, Hogers R, Bleeker M, et al. 1995. AFLP: a new technique for DNA fingerprinting. Nucleic Acids Research 23: 4407-4414.
77. Waser NM, Campbell DR. 2004. Ecological speciation in flowering plants. In: Dieckmann U, Doebeli M, Metz JAJ, eds. Adaptive speciation. Cambridge, UK: Cambridge University Press, 264-277.
78. Wu C-I. 2001. The genic view of the process of speciation. Journal of Evolutionary Biology 14: 851-865. (Pubitemid 34029787)
79. Wu C-I, Ting C-T. 2004. Genes and speciation. Nature Reviews Genetics 5: 114-122. (Pubitemid 38160278)
80. Xu S, Schluter PM, Scopece G, et al. 2011. Floral isolation is the main reproductive barrier among closely related sexually deceptive orchids. Evolution: International Journal of Organic Evolution: doi:10.1111/j.1558-5646. 2011.01323.x.
81. Zhivotovsky LA. 1999. Estimating population structure in diploids with multilocus dominant DNA markers. Molecular Ecology 8: 903-913.